Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat

doi:10.1016/S0306-4522(99)00262-6

Neuroscience

Volume 93, Issue 4, August 1999, Pages 1437-1447

https://doi.org/10.1016/S0306-4522(99)00262-6 Get rights and content

Abstract

In the rat, spinal autonomic neurons controlling penile erection receive descending pathways that modulate their activity. The paraventricular nucleus of the hypothalamus contributes oxytocinergic fibers to the dorsal horn and preganglionic sympathetic and parasympathetic cell columns. We used retrograde tracing techniques with pseudorabies virus combined with immunohistochemistry against oxytocin and radioligand binding detection of oxytocinergic receptors to evidence the oxytocinergic innervation of thoracolumbar and lumbosacral spinal neurons controlling penile erection. Spinal neurons labelled with pseudorabies virus transsynaptically transported from the corpus cavernosum were present in the intermediolateral cell column and the dorsal gray commissure of the thoracolumbar and lumbosacral spinal cord. Confocal laser scanning microscopic observation of the same preparations revealed close appositions between oxytocinergic varicosities and pseudorabies virus-infected neurons, suggesting strongly the presence of synaptic contacts. Electron microscopy confirmed this hypothesis. Oxytocin binding sites were present in the superficial layers of the dorsal horn, the dorsal gray commissure and the intermediolateral cell column in both the thoracolumbar and lumbosacral segments.

In rats, stimulation of the paraventricular nucleus induces penile erection, but the link between the nucleus and penile innervation remains unknown. Our findings support the hypothesis that oxytocin, released by descending paraventriculo-spinal pathways, activates proerectile spinal neurons.

Section snippets

Experimental procedures

All animal experiments have been carried out in accordance with the European Communities Council Directive of 24 November 1986 (86/609/EEC) for the care and use of laboratory animals. All efforts were made to minimize animal suffering and to reduce the number of animals used.

Neurophysin–oxytocin-immunoreactive fibers and pseudorabies-infected neurons

The distribution of NP-OT-IR fibers within the T12–L2 and L5–S1 spinal cords was comparable to that already reported at these levels by others using the same or different antibodies.42., 46. NP-OT-IR fibers were mainly distributed in the DH, DGC, IML and SPN of the spinal levels examined. In the DH, NP-OT-IR fibers were found in the superficial layers. From the medial edge of the DH and IML and SPN, NP-OT-IR fibers coursed towards the central canal area. Some NP-OT-IR fibers were seen in the

Discussion

Using transsynaptic transport of PRV from the corpus cavernosum, we identified a population of spinal neurons that project to the penis. Close appositions between NP-OT-IR fibers and those PRV-infected spinal neurons were evidenced in the autonomic nuclei of the thoracolumbar and lumbosacral spinal cords. Our results demonstrated an oxytocin innervation of spinal neurons involved in the control of erection. Stronger evidence for the oxytocin control of spinal proerectile neurons was provided by

Acknowledgements

This work was supported in part by a Grant from Institut pour la Recherche sur la Moelle Epinière (IRME) 1996–1998 to F.G. The authors gratefully acknowledge the contributions of Mrs E. Waltisperger for her excellent technical assistance, J. M. Gachon for photography and Dr D. Schovaert for his contribution to the acquisition of image analysis data. Confocal laser scanning microscope observation was realized with the contribution of P. Leclerc (INSERM IFR 21, Le Kremlin-Bicêtre, France).

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En conséquence ces informations peuvent influencer le choix du traitement dans cette région : les techniques de préservation nerveuse au cours d’exérèses carcinologiques ont été précisées, sur la base de ces résultats. Le contingent musculaire lisse, du muscle élévateur de l’anus est-il impliqué dans les troubles de la statique pelvienne, est-il accessible aux mêmes techniques de rééducation ?
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Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat

Abstract

Section snippets

Experimental procedures

Neurophysin–oxytocin-immunoreactive fibers and pseudorabies-infected neurons

Discussion

Acknowledgements

Neuromodulation of penile erection: an overview of the role of neurotransmitters and neuropeptides

Prog. Neurobiol.

Effects of oxytocin and vasopressin on thoracic sympathetic preganglionic neurons in the cat

Brain Res. Bull.

Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat

Cell. Tiss. Res.

Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis

J. Neurosci.

Participation of paraventricular nucleus of hypothalamus in central regulation of penile erection in the rat

J. Urol.

Autonomic innervation of reproductive organs: analysis of the neurons whose axons project in the main penile nerve in the pelvic plexus of the rat

Anat. Rec.

Electrophysiological evidence for oxytocin receptors on sympathetic preganglionic neurons—an in vitro study on the neonatal rat

Brain Res.

125I-Labelled d(CH2)5[Tyr(Me)2,Thr4,Tyr-NH29]OVT: a selective oxytocin receptor ligand

Eur. J. Pharmac.

Topography of the oxytocin receptor system in rat brain: an autoradiographical study with a selective radioiodinated oxytocin antagonist

J. chem. Neuroanat.

The influence of the paraventriculo-spinal pathway, and oxytocin and vasopressin on sympathetic preganglionic neurons

Brain Res.

Neural control of penile erection

Urol. Clin. North Am.

Neural control of penile erection in the rat

J. auton. nerv. Syst.

A preganglionic autonomic nucleus in the dorsal gray commissure of the lumbar spinal cord of the rat

J. comp. Neurol.

Preganglionic neurons in the sacral spinal cord of the rat: an HRP study

Neurosci. Lett.

Light microscopic localization of brain opiate receptors: a general autoradiographic method which preserves tissue quality

J. Neurosci.

Immunohistochemistry of synaptic input and functional characterizations of neurons near the spinal central canal

Brain Res.

Oxytocinergic innervation to the upper thoracic sympathetic preganglionic neurons in the rat

Expl Brain Res.

Intrinsic organization and monoaminergic innervation of the suprachiasmatic nucleus transplanted to adult rats. A light- and electron-microscopic study

J. Neurocytol.

Organization of lumbar spinal outflow to distal colon and pelvic organs

Physiol. Rev.

CNS cell groups involved in the control of the ischiocavernosus and bulbospongiosus muscles: a transneuronal tracing study using pseudorabies virus

J. comp. Neurol.

Central nervous system innervation of the penis as revealed by the transneuronal transport of pseudorabies virus

Neuroscience

Central control of penile erection

Int. J. Impot. Res.

Sympathetic afferent and parasympathetic preganglionic neurons labelled by horseradish peroxidase applied to the hypogastric nerve and the sacral sympathetic chain of the rat

Soc. Neurocsi. Abstr.

¹²⁵I-Labelled d(CH₂)⁵[Tyr(Me)²,Thr⁴,Tyr-NH₂⁹]OVT: a selective oxytocin receptor ligand